phil. trans. r. soc. lond. 2002, 357, 1481

8/3/2019 Phil. Trans. R. Soc. Lond. 2002, 357, 1481

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Published online 3 October 2002

The design and synthesis of artificial photosynthetic

antennas, reaction centres and membranes

T. A. Moore*, A. L. Moore and D. Gust

Department of Chemistry and Biochemistry and Centre for the Study of Early Events in Photosynthesis,

Arizona State University, Tempe, AZ 85287-1604, USA

Artificial antenna systems and reaction centres synthesized in our laboratory are used to illustrate that

structural and thermodynamic factors controlling energy and electron transfer in these constructs can

be modified to optimize performance. Artificial reaction centres have been incorporated into liposomal

membranes where they convert light energy to vectorial redox potential. This redox potential drives a

Mitchellian, quinone-based, proton-transporting redox loop that generates a H of ca. 4.4 kcal mol1

comprising pH ca. 2.1 and ca. 70 mV. In liposomes containing CF0F1ATP synthase, this system

drives ATP synthesis against an ATP chemical potential similar to that observed in natural systems.

Keywords: artificial photosynthesis; artificial antenna; artificial reaction centres

1. INTRODUCTION

Natural photosynthesis has inspired chemists to mimic

aspects of this successful energy-transducing process in

the laboratory. One of many approaches to the assembly

of an artificial reaction centre is to use synthetic pigments,

electron donors and electron acceptors that are related to

the natural pigments (chlorophylls, carotenoids and

quinones), but to employ covalent bonds in place of the

proteins that function as scaffolds, organizing the pig-

ments in the natural systems. Like the natural proteinmatrix, the covalent bonds of the artificial antennae and

reaction centres control the separations, angular relation-

ships and electronic coupling among the various active

moieties, and thus control the rates and yields of energy

and electron-transfer processes (Wasielewski 1992; Gust

et al. 1993a,b, 1999, 2000, 2001a,b; Gust & Moore 2000).

In 3, we will discuss biomimicry of the various functions

of carotenoids in photosynthesis. Later, in 5, the prep-

aration and function of artificial reaction centres will be

described. Finally, in 6 we will review progress in the

construction of artificial photosynthetic membranes.

2. CAROTENOIDS IN NATURAL PHOTOSYNTHESIS

(a) Carotenoid pigments as photosynthetic

antennae

As accessory light-harvesting pigments, carotenoids are

found in the chlorophyll-binding antenna proteins of

photosynthetic organisms where they absorb light in the

bluegreen spectral region and transfer energy to nearby

chlorophylls.

Carhv

1Car, (2.1)

* Author for correspondence ([email protected]).

One contribution of 21 to a Discussion Meeting Issue Photosystem II:

molecular structure and function.

Phil. Trans. R. Soc. Lond. B (2002) 357, 14811498 1481 2002 The Royal SocietyDOI 10.1098/rstb.2002.1147

1Car ChlCar 1Chl. (2.2)

Light energy collected in this way is funnelled to special

structures in the membranes, known as reaction centres,

where energy conversion to electrochemical potential

takes place. The unique photophysics of carotenoids (vide

infra) places severe constraints on aspects of the structure

of carotenoidchlorophyll-binding proteins that control

the interactions of the pigments. As described below,many of these structural constraints have been identified

in model systems by making systematic changes in the

linkages connecting carotenoid pigments to tetrapyrroles

and measuring the effect on energy-transfer rates and

yields. We begin with a brief review of carotenoid photo-

physics to set the stage for interpreting energy-transfer

experiments on model antenna systems.

(b) Carotenoid photophysics

This discussion applies to the genre of carotenoid pig-

ments having nine or more conjugated double bonds,

including oxy- and hydroxy-substituted compounds,

although there are certainly small differences between pig-ments. Carotenoid absorption of light in the 400550 nm

spectral region gives rise to their intense yelloworange

colour, a consequence of high extinction coefficients (ca.

105 M1 cm1) in this region. This strongly electric dipole

allowed transition is from the ground state (S0) to the

second excited singlet state (S2) of the carotenoid. As

expected for an upper excited singlet state, the S2 species

has a very short lifetime of 200 fs or less (Truscott 1990;

Shreve et al. 1991, 1992; Kandori et al. 1994; Macpher-

son & Gillbro 1998). Because of the short lifetime, the

quantum yield of fluorescence emission from this state is

very low (less than 104) in spite of the strongly allowed

nature of the transition and its correspondingly large radi-ative rate constant (ca. 109 s1). Surprisingly, this state

is important as an energy donor in photosynthesis

(Trautman et al. 1990; Ricci et al. 1996).


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1482 T. A. Moore and others Artificial antenna systems and reaction centres

The transition from S0 to the lowest excited singlet state

of carotenoids, S1, is electric-dipole forbidden (Kohler

1991) and is not observed in the usual single-photon

absorption experiment. It is readily populated by relax-

ation from S2. The lifetime of the S1 state, as measured by

transient absorption techniques, is ca. 1040 ps for most

carotenoids (Wasielewski & Kispert 1986; Trautman et al.

1990). The state decays essentially exclusively via internalconversion. Fluorescence from S1 is virtually undetectable

(quantum yield less than 104) and intersystem crossing

to the triplet state is not observed. The energy of the S1state is uncertain for most of the carotenoids involved in

photosynthesis because the forbidden nature of the

S0 S1 transition makes it difficult to detect.

Although carotenoid triplet states are not formed in

appreciable amounts by the usual intersystem crossing

pathway, they can be produced via triplettriplet energy

transfer from other species or by radical-pair recombi-

nation processes in artificial reaction centres (Gust et al.

1992; Liddell et al. 1997; Carbonera et al. 1998). Thus,

their transient absorption characteristics are well known(Mathis & Kleo 1973; Bensasson et al. 1976). Typically,

they have strong absorption maxima at about 540 nm. In

most organic solvents in the absence of oxygen, carotenoid

triplet states have lifetimes of 510 s. Phosphorescence

from these triplets has not been reported, and therefore

the energies of the carotenoid triplet states have not been

measured by direct optical means. Energy-transfer studies

have demonstrated that the energy of the lowest-lying car-

otenoid triplet is below that of singlet oxygen at ca. 1.0 eV.

Results from our laboratory were obtained using a hybrid

spectroscopiccalorimetric technique (photoacoustic

spectroscopy) that has located the lowest-lying triplet state

of a representative carotenoid (similar to the carotenoidmoiety of structure 10 (see Appendix A) except containing

one more conjugated double bond) at 0.65 0.04 eV

(Lewis et al. 1994). Thus, the expected origin of the phos-

phorescence would be ca. 1900 nm.

(c) Photoprotection

In the photosynthetic process, carotenoids have func-

tions that are ancillary to the basic energy-conversion reac-

tions and are crucial to the protection of photosynthetic

membranes from photochemical damage (Cohen-Bazire &

Stanier 1958; Sieferman-Harms 1987; Frank & Cogdell

1996). Under certain conditions, most photosynthetic

organisms unavoidably generate chlorophyll triplet excitedstates when exposed to light. Often, these are produced in

the reaction centre via recombination of charge-separated

states. Chlorophyll triplet states are excellent sensitizers

for formation of singlet oxygen from the oxygen ground-

state triplet as in the following equation:

3Chl 3O2Chl 1O2. (2.3)

Singlet oxygen, with an energy of ca. 1 eV above the

ground state, is a highly reactive species that can react

with and destroy lipid bilayer membranes and other vital

components of cells. Clearly, singlet oxygen production in

photosynthetic organisms is potentially injurious (Krinsky

1979; Cogdell & Frank 1993). Such organisms havedeveloped dual defence mechanisms based upon the low

energy of the carotenoid triplet state mentioned above.

Carotenes can quench chlorophyll triplet states at a rate

Phil. Trans. R. Soc. Lond. B (2002)

that precludes singlet oxygen generation via a triplet

triplet energy-transfer process (equation (2.4)). Addition-

ally, carotenoids can quench singlet oxygen itself through

energy transfer (equation (2.5)) or chemical reaction

(Foote et al. 1970).

3Chl CarChl 3Car, (2.4)

1O2 Car3O2

3Car. (2.5)

Because the carotenoid triplet state is much lower in

energy than singlet oxygen, it returns harmlessly to the

ground state with the liberation of heat.

From this overview, it is readily appreciated that carot-

enoids were selected by the evolving photosynthetic appar-

atus because of their unique photophysical properties.

Their strong absorption is closely matched to the

maximum of the solar flux, although their triplet levels are

well below the energy of singlet oxygen.

(d ) Regulation of photosynthesis by carotenoids

It has been found that carotenoid polyenes are involved

in a mechanism whereby some photosynthetic organisms

dissipate excess chlorophyll singlet excitation energy

(Yamamoto 1979; Demmig-Adams 1992; Yamamoto &

Bassi 1995; Horton et al. 1996). This process is sometimes

referred to as non-photochemical quenching because it is

measured by in vivo fluorescence spectroscopy of plant

leaves. It comes into play at high light levels and evidently

helps to protect the organism from light-induced damage.

Non-photochemical quenching is signalled by the conver-

sion of violaxanthin to zeaxanthin, but the details of the

quenching process are currently not understood.

3. CAROTENOIDS IN BIOMIMETIC SYSTEMS

(a) Mimicry of the antenna function of carotenoids

As indicated in equation (2.2), in order to act as

antennas for gathering light, carotenoid pigments must

transfer singlet excitation energy to nearby chlorophyll

molecules. Singlet energy transfer from carotenoid to

chlorophyll can occur by at least two different pathways.

At one limit, following absorption of light and internal

conversion from S2, the S1 level of the carotenoid is popu-

lated and then transfers energy to the Qy (S1) of the

chlorophyll. At the other limit, energy transfer from the

S2 level of the carotenoid to the Q x (S2) of the chlorophyllcompetes with internal conversion in the carotenoid. The

short lifetime of the S2 state of the carotenoid does not a

prioriexclude the second possibility. Indeed, detailed spec-

troscopic studies on the subpicosecond time-scale of the

pigment protein complexes that make up the light-

harvesting antennas of photosynthetic organisms indicate

that, in some cases, energy transfer from the carotenoid

to the chlorophyll or bacteriochlorophyll may occur from

the carotenoid S2 level rather that from the lower-energy

S1 excited state, as predicted by Kashas rule (Trautman

et al. 1990; Shreve et al. 1991; Koyama et al. 1996; Ricci

et al. 1996; Krueger et al. 1998). The two pathways are

shown schematically in figure 1.However, the complexity of the natural systems con-

taining multiple chromophores, coupled with the difficulty

of the measurements on such a short time-scale, make the


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Artificial antenna systems and reaction centres T. A. Moore and others 1483

energy(eV)

1.0

0

2.0

carotenoid tetrapyrrole

hv

Qx

Qy

S0S0(11Ag_

)

S1(21Ag_)

S2(11Bu

+)

Figure 1. Energy-level diagram showing both possible paths

for energy transfer from the excited singlet states of a

carotenoid to the S1 or S2 levels of a tetrapyrrole pigment.

pathway assignments uncertain. Structures 1 and 4 (see

Appendix A) are examples of simple, well-defined molecu-

lar dyads that were designed to help in the understanding

of the carotenoid to chlorophyll singletsinglet energy-

transfer process in natural systems.Transient absorption and fluorescence experiments on

structures 1 and 4 and the model pigments, structures 2,

3, 5 and 6 (see Appendix A), yielded convincing results

about the energy-transfer pathway (Macpherson et al.

2002). In structure 1, the lifetime of S2 was measured by

fluorescence upconversion to be 45 fs, whereas the S2 life-

time of model carotenoid 3 is 160 fs. The S 1 lifetime was

8 ps in both structures 1 and 3. Moreover, the S 1 rise time

for tetrapyrrole (moiety of dyad 1) was found to be 62 fs

by fluorescence upconversion. Therefore, only the carot-

enoid S2 state was quenched by the attached tetrapyrrole.

The observation that the time constant associated with the

decay of the energy donor (carotenoid S2) is consistentwith that associated with the energy arrival at the acceptor

(tetrapyrrole S1) solidly demonstrates the S2 energy-

transfer pathway. (The difference between carotenoid S2decay at 45 fs and tetrapyrrole S1 rise at 62 fs is due to

the delay associated with relaxation to the fluorescent state

in the tetrapyrrole.) Quantitatively, quenching of the caro-

tenoid S2 state from 160 fs to 45 fs by energy transfer

results in an efficiency of 70%, which matches that meas-

ured by steady-state fluorescence excitation spectroscopy.

Studies of dyad 4 illustrate that both pathways can be

active. In initial experiments on dyad 4, the attached tetra-

pyrrole was found to quench the carotenoid S2 state from

95 fs in model 6 to 28 fs, and the carotenoid S1 level from12 to 9 ps. The rise of the S1 level of the tetrapyrrole of

structure 4, as measured by fluorescence upconversion,

required a major exponential component (74%) of 41 fs


and a minor component (26%) of 4 ps. While the match

between the 9 ps decay of the carotenoid S1 and the 4 ps

rise component of the tetrapyrrole S1 is only qualitative,

these preliminary experiments do provide evidence that

both states can be energy donors. Taken together, the car-

otenoid S2 and S1 kinetic data give an overall quantum

yield of energy transfer of ca. 80%, in qualitative agree-

ment with that observed by steady-state fluorescence-excitation spectroscopy.

Why is the yield of the S1 pathway different in structures

1 and 4? There are undoubtedly subtle differences in the

electronic coupling between the chromophores (vide

supra) and the energy-transfer energetics are different. The

S1 level of the tetrapyrrole in stucture 4 is about 270 cm1

higher than that of structure 1. Considering this small

energy difference, the fact that the S1 carotenoid band is

expected to be rather broad (Frank et al. 1996) and that

the S1 levels of these carotenoids have not been measured

but should be similar, the role of thermodynamics in con-

trolling these energy-transfer processes remains speculat-

ive.

(b) Carotenoid antenna for non-photosynthetic

pigments

One of the clearest examples of the increased absorption

cross-section for a photochemical process provided by

carotenoid pigments is that observed in carotenoid

buckminsterfullerene dyad, structure 7 (see Appendix A)

(Imahori et al. 1995). The carotenoid absorption spec-

trum is distinct and much stronger than that of the under-

lying C60 bands. Upon excitation of the carotenoid moiety

of stucture 7 with a 150 fs pulse of 600 nm laser light, the

carotenoid radical cation forms in ca. 800 fs via photo-

induced electron transfer to the fullerene to yieldCC60. The charge-separated species has a lifetime of

ca. 500 ps and decays partially to the carotenoid triplet.

Excitation of the carotenoid pigment provides two routes

to the charge-separated species: energy transfer from the

carotenoid to the C60 followed by photoinduced electron

transfer to the C60 S1 and direct photoinduced electron

transfer from the carotenoid S1 level. Although the contri-

butions of the two pathways leading to CC60 could not

be separated, the overall quantum yield for the formation

of CC60 is unity. These results illustrate one way that

primary photochemistry with a high yield can occur upon

excitation of a carotenoid pigment, and keep the door

open to the suggestion that carotenoids can serve as bluelight photoreceptors (Quinones et al. 1996).

(c) Mimicry of the regulation of photosynthesis:

non-photochemical quenching

Regarding the role of carotenoid pigments in non-

photochemical quenching of photosynthesis mentioned in

1, it is interesting to compare structures 1 and 4. Both

demonstrate a high level of antenna function as measured

by energy-transfer efficiencies of 70 to 80%, which are

similar to those observed in many natural systems.

Regarding the tetrapyrrole singlet energies, the S1 level of

structure 1 is slightly lower than that of structure 4.

Although the carotenoid moieties in structures 1 and 4 aredifferent and their S1 levels are not known, there is no

evidence from the observed absorption into S2 that there

are significant differences in their singlet energy levels.


4/18


Interestingly, in structure 4 the tetrapyrrole fluorescence

is quenched (by the attached carotenoid) ca. 10-fold over

that of structure 1. This is consistent with a simple

description of the tetrapyrrole energetics in that energy-

transfer quenching from the tetrapyrrole S1 to the carot-

enoid would be more likely in structure 4 because the

tetrapyrrole S1 level is above that of the tetrapyrrole of

structure 1, and is therefore more likely to be above thatof the carotenoid S1. However, this interpretation is incon-

sistent with the carotenoid S1 state acting as an energy

donor in structure 4 and not in structure 1. If tetrapyrrole

to carotenoid energy transfer in structure 4 is thermodyn-

amically downhill, then carotenoid to tetrapyrrole energy

transfer must be uphill and is more uphill in structure 4

than in structure 1. Although we do not have an expla-

nation for the large quenching effect and enigmatic

energy-transfer behaviour, structures 1 and 4 do illustrate

that subtle changes in parameters such as the coupling

between the pigments, their redox levels and their spectro-

scopic energies can modulate and direct the energy flow

between carotenoids and tetrapyrroles.What is the role of energy or electron transfer in the

quenching of tetrapyrrole fluorescence by carotenoids?

In other model studies, the redox levels of a porphyrin

carotenoid dyad have been shown to influence the

quenching mechanism to the extent that electron transfer

from the carotenoid to the excited porphyrin was shown

to occur (Hermant et al. 1993). However, in a series of

carotenoidporphyrin dyads in which the number of con-

jugated carboncarbon double bonds in the carotenoid

moiety was systematically increased from 7 to 11, quench-

ing could not be assigned uniquely to either electron- or

energy-transfer processes (Cardoso et al. 1996). Unfortu-

nately, these model studies have not produced a definitiveanswer to the electron-/energy-transfer question.

(d ) Mechanistic considerations of energy transfer

Regarding the role of carotenoids as antenna pigments,

energy transfer from them to chlorophylls can be brought

about by a variety of interactions. If the distance between

the chromophores is larger than their transition dipole

lengths, if the transition dipoles have sufficient strength

and the correct orientation, and if the donor state has suf-

ficient lifetime (usually expressed as fluorescence quantum

yield), energy transfer may be described by the Forster

mechanism (Forster 1948). As the chromophores are

brought closer together, higher-order electrostatic termsmust be included in the electronic coupling matrix

elements. The inclusion of these terms can relax the need

for strong, dipole-allowed transitions and relatively long-

lived states in the donor and can account for the carot-

enoid S1 and S2 levels acting as donor states (Krueger et

al. 1998). If the chromophores are brought into van der

Waals contact so that there is orbital overlap between the

donor and the acceptor, the Dexter electron-exchange

mechanism becomes important.

The Dexter mechanism does not depend on dipole or

mutipole strengths and is the accepted mechanism for

triplettriplet energy transfer. How fast can Dexter-

mediated energy transfer be and to what extent do elec-tron exchange-based electronic coupling matrix elements

contribute to singlet energy transfer in these systems? In

dyads 1 and 2 and several other carotenoid-containing


multichromophoric molecules, energy transfer from the

triplet tetrapyrrole to populate the carotenoid triplet state

is remarkably fast. Due to kinetic constraints inherent to

these dyads, the actual rate cannot be determined

(Macpherson et al. 2002). In these model systems, the rise

time of the carotenoid triplet energy acceptor is the same

as the singlet lifetime of the tetrapyrrole triplet energy

donor. This indicates that intersystem crossing in thedonor is the rate-limiting step in the flow of energy from

the singlet of the donor to the triplet of the acceptor. In

other words, the true rise time of the triplet carotenoid is

much faster than intersystem crossing in the tetrapyrrole,

so that the carotenoid triplet is observed to rise with the

singlet lifetime of the tetrapyrrole.

The final answer to the second part of the question

awaits detailed quantum chemical calculations. In the

meantime, it has been addressed experimentally in one

study of three isomeric carotenoporphyrins in which singlet

singlet energy-transfer efficiency (albeit at much lower

efficiency than observed in dyads 1 and 2) and triplet

triplet energy-transfer rates were found to depend in thesame way on the electronic structure of the interchromo-

phore linkage group (Gust et al. 1992). Because the triplet

energy-transfer process is mediated by the linkage group

via the Dexter mechanism, the simplest interpretation is

that in those dyads the singlet energy transfer is also elec-

tron-exchange mediated.

4. EVOLUTION OF CAROTENOID

ANTENNA/PHOTOPROTECTIVE FUNCTION

IN PHOTOSYNTHESIS

One may assume that carotenoids were selected by the

evolving photosynthetic apparatus because of their uniquephotophysical properties. Three properties can be ident-

ified that stand out in this regard: (i) a highly allowed

absorption band in the 450 to 500 nm range, where the

solar flux is high for efficient light harvesting; (ii) an S1energy level that is highly forbidden (vide supra); and (iii)

a lowest-excited triplet state that is well below the energy

of singlet oxygen (1g, 0.98 eV) so that equation (2.5) is

irreversible. Notwithstanding the fact that the highly

allowed absorption band near the solar irradiance

maximum accounts for between 25 and 50% of the sun-

light that drives photosynthesis on the earth, the crucial

role of carotenoids in photosynthesis today is undoubtedly

to protect photosynthetic organisms from the deleteriouseffects of singlet oxygen.

It is interesting to speculate about the evolutionary ori-

gin of photoprotection and the link between photoprotec-

tion and the highly forbidden carotenoid S1 level (Moore

et al. 1990, 1994). From the earliest photosynthetic organ-

isms until the evolution of oxygen production (2.5ca. 3.5

billion years ago), atmospheric oxygen levels were

extremely low; there would have been no need for protec-

tion from singlet oxygen under these conditions. However,

it is almost certain that photosynthetic organisms evolving

during this time used carotenoids as light-harvesting pig-

ments. In order to do so, chlorophyll and carotenoid bind-

ing proteins evolved in which singlet energy transfer fromcarotenoids to chlorophylls was efficient. Because of the

forbidden nature of the carotenoid S1 level, efficient

energy transfer required extensive electronic coupling


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6/18


absorption and emission spectra. The fullerene absorbs

throughout the visible spectrum with a threshold at ca.

710 nm; its extinction coefficients in the visible region are

much lower than those of the porphyrin. The absorption

spectra are essentially linear combinations of those of the

component chromophores, which means that the spectra

show no evidence of strong electronic interaction of the

chromophores. Cyclic voltammetric studies on structure9 (see Appendix A) and model compounds allow esti-

mation of the energy of PC60 as 1.58 eV above the

ground state in polar solvents.

Analysis of time-resolved fluorescence and absorption

data for the dyads and appropriate model compounds

allows calculation of rate constants for various photo-

chemical processes. In toluene, 1PC60 of structure 9

decays by singletsinglet energy transfer (step 1 in figure

2; k1 = 4.5 1010 s1) to yield P1C60, which undergoes

intersystem crossing to the triplet state. No photoinduced

electron transfer is observed. In polar solvents such as

benzonitrile, 1PC60 decays by a combination of photoind-

uced electron transfer by step 2 (k2 = 1.8 1011

s1

) togive PC60 and singlet energy transfer by step 1

(k1 = 7.1 1010 s1). The P1C60 formed in this manner

or by direct absorption of light decays by photoinduced

electron transfer step 3 to also yield the PC60 state

(k3 = 1.3 1010 s1). The charge-separated state is easily

identified using transient absorption spectroscopy by the

absorption of the porphyrin radical cation in the 600

700 nm region and the fullerene radical anion at ca.

1000 nm. The overall quantum yield of charge separation

via both pathways is 0.99. The PC60 state decays

by charge recombination to the ground state with

k4 = 3.4 109 s1.

In general, the studies of photoinduced electron transferin porphyrinfullerene dyads have shown that charge-

separated states are produced in high yield, and have long

lifetimes relative to those of similar porphyrinquinone

systems (Liddell et al. 1994; Kuciauskas et al. 1996). For

example, a comparison of the photochemistry of a porphyrin

fullerene dyad with that of a structurally related porphyrin

quinone dyad shows that in tetrahydrofuran solution,

photoinduced electron transfer in the C60-dyad occurs

with a rate constant ca. six times larger than that in the

quinone-based dyad, even though the latter one has a driv-

ing force that is larger by 0.28 eV (Imahori et al. 1996).

But the most remarkable difference is in the charge recom-

bination reaction. In the quinone-based dyad, this reac-tion occurs with a rate constant of ca. 25 times greater

than in the C60-based dyad. The difference in rate con-

stants has been ascribed to a significantly smaller reorgani-

zation energy for the large, diffuse fullerene radical anion

than for the quinone radical anion, where the negative

charge is mostly concentrated in the region of the oxygen

atoms (Imahori et al. 1996; Guldi 2000; Kuciauskas et al.

2000). Because of the small , the maximum of the Mar-

cus curve occurs at a numerically smaller G, shifting

the more exergonic recombination reaction well into the

Marcus inverted region and slowing recombination.

(c) Triad-based artificial reaction centresDyad systems can generate charge separation with a

quantum yield of essentially unity while preserving a large

part of the photon energy as intramolecular redox poten-


tial. However, rapid charge recombination to the ground

state, which usually occurs on the subnanosecond time-

scale, releases the stored energy as heat; it is difficult to

devise intermolecular energy-conserving processes that

can compete with this degradation.

In the early 1980s, we designed an artificial photosyn-

thetic reaction centre that overcomes this problem by

using a multistep electron-transfer strategy such as thatfound in natural reaction centres (Moore et al. 1984).

Recently, we have designed a series of triad arti ficial reac-

tion centres based on the dyads described above. These

constructs illustrate that careful consideration of the ther-

modynamic and electronic factors controlling electron

transfer can result in artificial reaction centres that gener-

ate charge-separated states that rival those from natural

reaction centres in quantum yield, energetics and lifetime.

(d ) Photochemistry of fullerene-based triad

artificial reaction centres

As described above, photoinduced electron-transfer

studies in porphyrinfullerene dyads demonstrated thatcharge-separated states can be produced in high yield and

that they have long lifetimes relative to quinone-containing

dyads. These properties of fullerene systems indicate that

they might be ideal components of more complex systems,

where slow charge recombination would favour evolution

of a charge-separated state into a longer-lived species via

multistep electron transfers similar to the processes

observed in the reaction centres of photosynthetic organ-

isms.

In 1997, we reported a next step in the evolution of

such molecules in the form of carotene (C) porphyrin (P)

fullerene (C60) triad 10 (Gust et al. 1997; Liddell et al.

1997; Kuciauskas et al. 2000). Other triads based on C60have subsequently been reported (Luo et al. 2000). The

photochemistry of this triad may be discussed with refer-

ence to figure 3, which shows the relevant high-energy

states and decay pathways. Time-resolved spectroscopic

studies have shown that at ambient temperatures in 2-

methyltetrahydrofuran solution, excitation of the porphy-

rin moiety yields C1PC60, which decays in 10 ps by pho-

toinduced electron transfer to the fullerene to generate

CPC60 (step 3 in figure 3; k3 = 1.0 1011 s1). Also,

the fullerene excited singlet state accepts an electron from

the porphyrin to yield CPC60 (k2 = 3.1 1010 s1).

The overall quantum yield of CPC60 by these two

pathways is essentially unity. Secondary electron transferfrom the carotenoid (step 4) competes with charge recom-

bination by step 7 to give the final CPC60 charge-

separated state. The rise time of this state is 80 ps and the

overall yield is ca. 0.14, as determined by the comparative

method. The CPC60 state decays in 170 ns exclus-

ively by charge recombination to produce the carotenoid

triplet state (step 9, t = 0.13). Decay of3CPC60 occurs

in 4.9 s (k15 = 2.0 105 s1). Even in a glass at 77 K,

CPC60 is formed from C1PC60 with a quantum

yield of ca. 0.10 and again decays to give 3CPC60. The

fullerene triplet, formed from CP1C60 (step 10) through

normal intersystem crossing, is also observed at 77 K.

Importantly, charge recombination to form a tripletspecies in triad 10 provides a spectroscopic label to follow

the flow of triplet energy and the spin dynamics in model

photosynthetic reaction centres. The spin-polarized EPR


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...

0

.

Figure 3. Energy-level diagram showing relevant high-energy states and energy and electron-transfer decay pathways for triad

10. Triads 11 and 12 differ in the energies of certain charge-separated states as fully described in 5d. The singlet radical-pairstate 1(CPC60) is shown along with the three triplet radical-pair states

3(CPC60). The splittings of the triplet

radical-pair state energies are not to scale.

signal of the final charge-separated state, CPC60,

was observed and simulated (Hasharoni et al. 1990). The

fact that both electron-transfer steps in structure 10 occur

even in a glassy matrix at 77 K has made it possible to

observe some unusual and biologically relevant triplet

triplet energy-transfer phenomena in the triads (Gust et al.

1997). In triad 10, triplet energy is transferred from the

fullerene moiety of CP3

C60 (generated by intersystemcrossing) to the carotenoid polyene (step 11 followed by

step 12), yielding 3CPC60. The transfer has been stud-

ied both in toluene at ambient temperatures and in 2-

methyltetrahydrofuran at lower temperatures. The energy

transfer is an activated process (step 11), with

Ea = 0.17 eV. This is consistent with transfer by a triplet

energy-transfer relay, whereby energy first migrates from

CP3C60 to the porphyrin (step 11), yielding C3PC60

in a slow, thermally activated step. Rapid energy transfer

from the porphyrin triplet to the carotenoid (step 12) gives

the final state. Triplet relays of this general kind have been

observed in photosynthetic reaction centres and are part

of the system that protects the organism from damage bysinglet oxygen, whose production is sensitized by chloro-

phyll triplet states (Gust et al. 1993a; Krasnovsky et al.

1993).

As explained above, the CPC60 state decays at

77 K to give the carotenoid triplet. EPR investigation of

the signal from this triplet state shows that the spin polar-

ization of 3CPC60 is characteristic of a triplet formed by

charge recombination of a singlet-derived radical pair.

The kinetics of the decay of 3CPC60 to the ground state

were also determined and the decay constants for the three

triplet sublevels were measured. Similar spin states and

dynamics, which are the signature of radical-pair recombi-

nation reactions, have been observed in photosyntheticreaction centres but are unique to structure 10 (and close

relatives) in the area of photosynthetic model systems

(Carbonera et al. 1998). To aid our interpretation of the


EPR spectra of the triads, we carried out several other

studies on the EPR properties of caroteneporphyrin

dyads (Carbonera et al. 1997a,b). The generation in triad

10 of a long-lived charge-separated state by photoinduced

electron transfer, the low-temperature electron-transfer

behaviour and the formation of a triplet state by charge

recombination are phenomena heretofore observed mostly

in photosynthetic reaction centres, rather than in modelsystems.

Although triad 10 mimics some of the important fea-

tures of photosynthetic electron transfer, the quantum

yield of the final state is rather low (0.14). The initial

CPC60 state is formed with a quantum yield

approaching unity, but charge recombination to the

ground state is more rapid than electron transfer from the

carotenoid to yield the final state. In order to overcome

this problem, triad 11 was designed. It differs from struc-

ture 10 mainly in the nature of the carotenoid-to-porphyrin

linkage (Kuciauskas et al. 2000). A major effect of this

structural change is to increase the electron-donating

ability of the carotenoid by 0.18 eV, although it alsoaffects the electronic coupling. In addition, the change

raises the energy of CPC60 by 0.05 eV relative to

structure 10. In accord with Marcus theory, these ener-

getic changes increase the thermodynamic driving force

and rate constant for formation of CPC60 from

CPC60 (step 4). They also slightly increase the driv-

ing force for charge recombination of CPC60 (step

7). However, as this reaction occurs in the Marcus

inverted region, the rate of recombination is slowed. The

overall result is that the yield of CPC60 is 0.88 in

structure 11 (see Appendix A).

In order to retard the rate of charge recombination of

CP

C

60 even more, and thereby increase the yield ofCPC60, triad 12 was synthesized (Bahr et al. 2000).

In structure 12 (see Appendix A), the octaalkylporphyrin

serving as the primary donor was replaced with a tetra-


8/18


phenyl-based porphyrin that increases the energy of P

by ca. 200 mV. Therefore, in structure 12, the charge

recombination process (step 7) from CPC60 is even

further in the Marcus inverted region and thereby slower,

allowing the forward reaction yielding the final charge-

separated species CPC60 to better compete with it.

Moreover, this change increases the driving force for hole

transfer from the porphyrin radical cation to the carot-enoid (step 4), which is in the Marcus normal region and

therefore is accelerated. The combination of a faster for-

ward reaction combined with a slower recombination

reaction from the intermediate CPC60 results in a

measured quantum yield for the formation of CP

C60 of ca. 100% in triad 12.

The availability of structures 10, 11 and model com-

pounds has allowed the investigation of the effects of tem-

perature and solvent on the various electron-transfer steps.

For example, electron-transfer dynamics on a very short

time-scale as a function of solvent were studied in triad

10 and in a related porphyrinfullerene dyad using sub-

picosecond transient absorption techniques (Kuciauskas etal. 1998a). After porphyrin photoexcitation of the dyad,

electron transfer to the fullerene was observed, yielding

PC60. In toluene, this state recombines to give the ful-

lerene first-excited singlet state, leading to fullerene singlet

sensitization by an unusual two-step electron-transfer

mechanism. This is somewhat analogous to the delayed

fluorescence observed in natural reaction centres when

secondary electron transfer is blocked. In polar solvents,

structure 10 undergoes the electron-transfer process men-

tioned previously to produce CPC60. The solvation

dynamics of this state were investigated by monitoring car-

otenoid radical cation absorption band bathochromic

spectral shifts. Picosecond solvation processes were

observed in six solvents, with solvation lifetimes ranging

from 0.4 to 35 ps. In all solvents, electron-transfer rates

were slower than solvation rates, but the difference is not

large. It was also observed that when solvation of the caro-

tenoid radical cation is faster, electron transfer is more

rapid.

An extensive comparison of the effects of temperature

and solvent on triads 10 and 11 allowed several generaliza-

tions (Kuciauskas et al. 2000). Rate constants for photoin-

duced charge separation are much larger than those for

charge recombination. In addition, the rate constants of

the various electron-transfer reactions in structure 11

depend only weakly on temperature and solvent. The yield

of CPC60 in structure 11 is essentially independent

of temperature down to 8 K. The rate constants for photo-

induced electron transfer and for charge recombination of

CPC60 do not change drastically when the solvent

changes from a fluid solution to a rigid glass. Charge

recombination of CPC60 also has some unusual fea-

tures. In non-polar solvents or frozen glasses down to 8 K,

charge recombination in structures 10 and 11 yields only

the carotenoid triplet state. However, in polar solvents,

charge recombination in structure 11 yields only the sing-

let ground state (step 8). The rate of charge recombination

of C

PC

60 in both structures 10 and 11 is temperature-dependent down to ca. 170 K, and temperature inde-

pendent thereafter. The temperature-independent region

is attributed to nuclear tunnelling.


(e) An artificial antennareaction centre complex:

a molecular hexad

Antenna function in photosynthesis has been mimicked

in artificial systems of covalently linked arrays. For

example, metalated and free base porphyrins have been

linked with alkyne units to form dimers, trimers, tetra-

mers, pentamers and more complex supermolecules that

absorb light and rapidly and efficiently transfer singletexcitation to energy sinks such as a free base porphyrin

moiety (Seth et al. 1994, 1996; Bothner-By et al. 1996;

Hsiao et al. 1996; Wagner et al. 1996a; Strachan et al.

1997; Lammi et al. 2000). Molecules of this type have

been designed to act as photonic wires and gates

(Wagner & Lindsey 1994; Wagner et al. 1996b). Other

porphyrin arrays, some of them including more than one

hundred porphyrin units, with demonstrated or potential

antenna function have been reported (Van Patten et al.

1998; Cho et al. 2000).

Because of the progress made in the mimicry of both

photosynthetic antennas and reaction centres, a logical

next step would be to link an artificial light-harvestingarray with a synthetic reaction centre to produce a func-

tional energy-conversion assembly. Indeed, a model pho-

tosynthetic antenna consisting of four covalently linked

zinc tetraarylporphyrins, (PZnP)3PZnC, covalently joined

to a free base porphyrinfullerene artificial photosynthetic

reaction centre, PC60, to form (PZnP)3PZnCPC60,hexad 13, has been reported (Kuciauskas et al. 1999).

In order to evaluate the performance of hexad 13, rate

constants were extracted from time-resolved spectroscopic

data. The time-resolved fluorescence and absorption data

yield a time constant of 700 ps that is associated with the

zinc porphyrin moieties. The shortening of the zinc por-

phyrin singlet lifetime from 2.4 ns in tetrad (PZnP)3PZnCto give a 700 ps component in a model pentad, (PZnP)3

PZnCP and structure 13 (see Appendix A) is a result of

singletsinglet energy transfer from the zinc porphyrins to

the free base porphyrin. In structure 13, fluorescence from

the free base porphyrin is quenched from its usual lifetime

ofca. 10 ns to such a degree that fluorescence is no longer

observable. The picosecond transient absorbance results

yield additional time constants of 3 ps, 12 ps and 1.3 ns.

The rate constant for photoinduced electron transfer

and the charge recombination rate constant are directly

observed experimentally. The reciprocal of the 3 ps time-

constant detected in the transient absorption experiments

is the rate constant for photoinduced electron transfer.This assignment is verified by the results for a model P

C60 dyad, where the same value was obtained for the rate

constant for photoinduced electron transfer. The charge

recombination of (PZnP)3PZnCPC60 is associated

with the 1.3 ns decay component observed in transient

absorption, as demonstrated by the spectral stamp of the

fullerene radical anion with absorption in the 1000 nm

region. This lifetime is within a factor of 2.5 of the lifetime

observed for the PC60 in a model dyad (480 ps).

The values for the singlet energy-transfer rate constants

between zinc porphyrins and between the central zinc por-

phyrin and the free base porphyrin do not appear directly

in the experimental decays. A kinetic model wasdeveloped to interpret the spectroscopic data and a sol-

ution of a set of rate differential equations using the exper-

imentally measured lifetimes of 12 ps and 700 ps as


9/18


constants yields values of 50 ps for the rate constant for

energy transfer between metal porphyrins and 240 ps for

the rate constant for energy transfer between the zinc and

free base porphyrins. The value thus obtained for the rate

constant for energy transfer between metal porphyrins is

in excellent agreement with the results of Hsiao and

coworkers who measured a rate constant of 53 ps for sing-

let energy transfer between two zinc porphyrins in a lineartrimeric array of zinc porphyrins with diphenylethyne link-

ages very similar to those in structure 13 (Hsiao et al.

1996).

The singletsinglet energy transfer between the central

zinc porphyrin in the antenna of structure 13 and the free

base porphyrin is slow (240 ps) compared with that

between the zinc porphyrins (50 ps). Thus, the energy

transfer between the central zinc porphyrin and the free

base porphyrin creates a bottleneck that limits the quan-

tum yield of the final charge-separated state (PZnP)3PZnC

PC60.

The quantum yield of (PZnP)3PZnCPC60 is wave-

length dependent. Based on light absorbed by the freebase porphyrin, the yield is unity, due to the very large

rate constant for photoinduced electron transfer. The

quantum yield based on excitation of the zinc porphyrins

in the antennas is 0.70. In this process, the light-gathering

power of the system is increased considerably at many

wavelengths, as four zinc porphyrin moieties feed exci-

tation energy to the reaction centre. In hexad 14 structural

modifications to increase the electronic coupling between

PZnCP and the thermodynamic driving force for selected

electron-transfer steps were carried out to improve the

performance of this device in terms of lifetime and quan-

tum yield of the final charge-separated state (Kodis et al.

2002).Hexad 14 differs from structure 13 in several important

ways. By changing the primary donor porphyrin from the

free base octaalkylporphyrin of structure 13 to a free base

tetraphenyl-type porphyrin, the energy of the correspond-

ing radical cation is increased by ca. 200 mV. This pro-

vides an additional thermodynamic driving force for hole

transfer from the primary donor to the Zn porphyrins act-

ing as the antenna. Evidence for this is provided by the

appearance in the transient spectra of the Zn porphyrin

radical cation in 380 ps and greatly increased lifetime of

the charge-separated state in structure 14 (see Appendix

A) of up to 24 s (solvent dependent) versus 1.3 ns in

structure 13. As mentioned above, this change of severalorders of magnitude in lifetime is characteristic of multi-

component systems in which a secondary electron-transfer

step results in formation of a neutral chromophore separ-

ating electron-hole pairs. Increasing the energy of the por-

phyrin radical cation also lowers the driving force for

photoinduced electron transfer from the primary donor to

the C60 and, indeed, charge separation is slower, 25 ps in

structure 14 versus 3 ps in structure 13, because this step

is in the Marcus normal region. Twenty-five picoseconds

is still sufficiently fast so that the yield of the photoinduced

electron-transfer process, competing against fluorescence

and intersystem crossing, is not measurably changed

from 100%.A second consequence of the change to a tetraphenyl-

based porphyrin as the primary donor in hexad 14 is that

there are no methyl groups at the beta positions. This


allows a more coplanar conformation between the central

Zn porphyrin of the antenna and the primary donor,

which increases the electronic coupling and results in

much faster singlet energy transfer. The time for this step,

which was 240 ps in structure 13 and limited the overall

quantum yield of energy transfer, is reduced to 30 ps in

structure 14, giving an energy-transfer yield of unity.

Therefore, the quantum yield of photoinduced electrontransfer from the primary donor to the C60 in structure

14 is essentially 100%, regardless of which porphyrin is

initially excited.

In addition to the changes noted above in thermodyn-

amics and conformation that are brought about by chang-

ing the primary donor from an octaalkylporphyrin to a

tetraphenyl-based porphyrin, there are electronic effects

arising from changes in the molecular orbital nodal pattern

of the two porphyrins. Specifically relevant to hole transfer

from the primary donor to the Zn porphyrin of the

antenna, the HOMO of the octaalkylporphyrin has a node

at the meso positions whereas the HOMO of the

tetraphenyl-based porphyrin has amplitude at the mesopositions. Because the meso position is the attachment

point of the Zn porphyrin array to the primary donor por-

phyrin, and because the HOMOs are involved in hole

transfer, this aspect of the electronic-coupling term should

be larger in structure 14 than in structure 13. The result of

improved thermodynamics for hole transfer and increased

electronic coupling due to conformation and orbital

effects is hole transfer from the radical cation of the pri-

mary donor to the antenna in 380 ps. This is sufficiently

fast for this step to have a yield of close to unity so that

the overall quantum yield of long-lived charge-separated

species in hexad 14 is near 100%.

6. ARTIFICIAL PHOTOSYNTHETIC MEMBRANES

Molecular triad 15, which consists of a porphyrin chro-

mophore (P) bound covalently to a naphthoquinone

derivative (NQ) and a carotenoid electron donor (C), was

designed both to undergo multistep electron transfer and

to organize itself in a bilayer lipid membrane. These two

characteristics are discussed below.

Excitation of the porphyrin moiety of structure 15 (see

Appendix A) (the photophysics of structure 15 is not

strongly dependent on the ionization state of the car-

boxylate group) leads to C1PNQ, which decays by pho-

toinduced electron transfer to give CP

NQ

with aquantum yield near unity. Competing with charge recom-

bination, a second electron transfer from the carotenoid

to the porphyrin radical cation occurs, yielding a C P

NQ charge-separated state. In this state, the radicals are

separated by the neutral porphyrin moiety and therefore

charge recombination is slower by several orders of magnitude

than that of a comparable dyad. We have used this strategy

in a variety of other reaction-centre mimics (vide supra),

some of which rival the natural systems in terms of quan-

tum yield, fraction of energy stored and lifetime for charge

separation (Gust & Moore 1991; Gust et al. 1993b).

It has been demonstrated that, under certain conditions,

triad 15 inserts unidirectionally into a liposomal phospho-lipid bilayer membrane (Steinberg-Yfrach et al. 1997).

How can this observation be rationalized? Triad 15 is

highly amphiphilic due to the hydrophobic carotenoid pig-


10/18


C

C C

C

C

C

C

C

6

1

Q s H

7

QsH+

Qs

5

Qs

Qs

+

Qsh

v

+

+

_ 2

+

Q s

3

+

Q s H

+

4

P P

H

QQ

H2O, buffer

Q

P

P

P

P

Q

Q

Q

Q

P

P

Q

_

H

pyraninetrisulphonate

9-aminoacridine

8-anilinonaphthalene-1-sulphonic

acid

H2O,

or

or

buffer

.

.

...

.

.

.

Figure 4. Steps 17 illustrate a minimum set of proposed

elementary processes involved in the redox loop-based

proton translocation across a liposomal bilayer membrane.

ment distal to the carboxylate group that is attached to

the naphthoquinone. When a small amount of structure

15 (dissolved in a suitable solvent such as tetrahydrofuran)

is added to an aqueous solution of liposomes, the amphi-

philic molecules associate with the membrane. It is prob-

able that the most stable association features thehydrophobic carotenoid moiety in the low-dielectric

interior of the bilayer and the hydrophilic carboxylate

group at or near the aqueous interface. Because structure

15 is added from the bulk aqueous phase on the outside

of the liposomal bilayer, the expected initial arrangement

would be vectorial, with the majority of triads having their

carboxylate-bearing naphthoquinones near the bulk aque-

ous phase as shown schematically in figure 4. The ener-

getic cost of transporting the carboxylate across the bilayer

would slow, but not prevent, flip-flop diffusion that would

ultimately randomize the orientation.

(a) Artificial proton pumpThe availability of artificial reaction centres that self-

assemble vectorially into bilayer lipid membranes makes

it possible to design a proton pump that will generate a

transmembrane gradient in proton electrochemical poten-

tial, the next step in converting solar energy to a biologi-

cally useful form (Steinberg-Yfrach et al. 1997). In order

to couple the vectorial redox potential in the species C

PNQ to proton translocation, a lipophilic shuttle quin-

one, Qs, was incorporated into the liposomal bilayer where

it functions as a redox loop to shuttle protons across the

bilayer. A proposed mechanism for this proton translo-

cation is shown diagrammatically in figure 4.

To begin with, excitation of structure 15 generates theCPNQ charge-separated state via the multistep

electron-transfer process described above. The shuttle

quinone Qs is more easily reduced than the naphthoqui-


none of the triad and therefore accepts an electron from

the charge-separated state to generate the Qs radical

anion, which is basic enough to accept a proton from the

nearby external aqueous phase. The resulting neutral

semiquinone is lipid soluble and diffuses within the lipo-

philic part of the bilayer. When it encounters a carotenoid

radical cation near the internal aqueous phase, it is readily

oxidized, yielding a protonated quinone, QsH

. Thisstrong acid releases a proton to the nearby interior aque-

ous volume, thereby lowering the pH inside the liposome

and regenerating the components of the proton pump. In

other words, the vectorial redox potential of CPNQ

drives a redox loop in which the reduced (protonated)

form of Qs carries protons inwards and the oxidized

(unprotonated) form of Qs completes the loop by equilib-

rating across the membrane. The specific details of the

proton-pumping photocycle may differ somewhat from

this simple picture, but figure 4 describes the basic fea-

tures of the system.

Proton import has been monitored by several methods.

A pH-sensitive fluorescent dye, pyraninetrisulphonate, wastrapped inside the liposomes, or 8-aminoacridine was used

to measure pH directly, or 8-anilinonaphthalene-1-

sulfonic acid was used to measure the transmembrane

electrical potential . Illumination of the liposomes with

light absorbed by the porphyrin moiety of structure 15

leads to a change in the fluorescence properties of these

dyes that signals import of protons into the liposomes. A

H of ca. 4.4 kcal mole1 comprised of pH ca. 2.1

and ca. 70 mV is attained after a few minutes of

irradiation with less than 0.1 mW of red light. The pH and

gradients thus generated can be relaxed by addition of

an ionophore such as FCCP. The photochemical import

of protons is enhanced by the addition of potassium andvalinomycin, which presumably reduce the uncompen-

sated charge buildup () in the intraliposomal volume.

Conversely, increasing the buffer concentration inside the

liposomes decreases the magnitude ofpH and results in

the generation of a greater . Thus, a photocyclic trans-

membrane proton pump has been assembled.

(b) ATP synthesis by the artificial membrane

Proton motive force is a basic form of biological energy

that is used to drive most energy-requiring reactions in

living organisms. Most importantly, it is used to power the

synthesis of ATP. Having prepared a light-driven trans-

membrane proton-pumping system, we have used it topower ATP synthesis in a biomimetic fashion. In nature,

ATP is synthesized by F0F1ATP synthase, an enzymatic

system that spans the lipid bilayer. Protons pass through

the enzyme from one side of the membrane to the other

in the direction of the pH gradient and the energy pro-

vided by relaxation of the electrochemical potential gradi-

ent is used to synthesize ATP from ADP and Pi.

Conditions for extraction of the CF0F1ATP synthase

from spinach chloroplast thylakoids and reconstitution of

the functional enzyme into liposomes have been

developed. Using this methodology, the enzyme has been

reconstituted into liposomes containing the components

of the light-driven proton pump discussed above(Steinberg-Yfrach et al. 1998).

The system is shown as a diagram in figure 5. The lipo-

somes were formed from a 10 : 1 mixture of egg phosphat-


11/18


OO

O

OO

O

.

triad 15

H+

Q

P

C

P

Q

C

hv

QS

+

.HQs

._

H+

4H+

ADP + Pi

Fo

F1

4H+

ATP

CF0F1-ATP synthase

intraliposomal volume

Figure 5. Schematic diagram of CFoF1 ATP synthase inserted into a liposomal membrane containing the components of the

artificial reaction centre and redox loop-based proton pump. The enzyme is reconstituted into the membrane with the

nucleotide binding sites in the external aqueous phase.

idylcholine and egg phosphatidic acid containing 20%

cholesterol. The ATP synthase was inserted into the

bilayer with the ATP-synthesizing portion of the enzyme

extending out into the external aqueous solution. The

constituents of the proton pump were incorporated as

described above. Thioredoxin (10 M) was added to acti-

vate the enzyme and ADP, Pi and an initial amount of

ATP were added to the external phase. The aqueous

phases were adjusted to a pH of 8 prior to illumination.

The liposomes were illuminated for various periods of

time with laser light at 633 nm, which was absorbed only

by the triad. Illumination was terminated, and the ATP

produced was measured using a calibrated luciferin/luciferase assay, which is based on the luminescence of

oxyluciferin. The amount of ATP produced during each

period of illumination was determined; typical results are

presented graphically in figure 6.

In order to establish that this increase was indeed due

to ATP synthesis driven by light-induced proton motive

force, several control experiments were performed. As

shown in figure 6, no ATP was synthesized when 1 M

FCCP, the proton ionophore mentioned above, was

added to the system, making the membrane permeable to

protons. Addition of 2 M tentoxin, which is a specific

inhibitor of CF0F1ATP synthase, halted ATP synthesis,

as did omission of the shuttle quinone Qs or ADP. Like-wise, omission of Pi, triad 15 or ATP synthase abolished

the effect.

At low levels of illumination, where ATP synthesis was

limited by light absorption, it was found that one ATP

molecule was synthesized for every 14 photons incident

on the sample. As ca. 50% of the light was absorbed by

the scattering liposome solutions, this corresponds to a

quantum yield of ca. 0.15. Assuming that four protons

must be transported out of the liposome by ATP synthase

per molecule of ATP produced, the yield of the proton

pump must be ca. 0.6. It should be noted that the lipo-

somes used for ATP synthesis were of a different size and

lipid mix from those used in the proton translocationexperiments discussed in the previous section ( 6a), and

that ca. 1000 triad 15 molecules could be incorporated

into one proteoliposome. In the proton translocation


ATP

produced(molATP1

011)

Figure 6. The synthesis of ATP as a function of illumination

time at different ratios of [ATP]/[ADP] (triangles, [ATP] =

[ADP] = 0.2 mM and [Pi] = 5 mM; filled circles, [ATP] =

0.2 mM, [ADP] = 0.02 mM and [Pi] = 5 mM. Also shown

are results for control experiments showing that ATP was

not synthesized (open circles, 1 M FCCP; filled triangles,2 M tentoxin; diamonds, [Qs] = 0; open squares, [ADP] = 0.

experiments, only ca. 40 triad molecules were present in

each liposome.

As illustrated in figure 6, the liposome system can syn-

thesize ATP against a considerable ATP chemical poten-

tial. Under the conditions of 0.2 mM ATP, 0.02 mM

ADP and 5 mM Pi shown in figure 6, ATP is synthesized

against a chemical potential of ca. 12 kcal mol1. Thus,

the system is converting light energy to chemical potential,

rather than simply catalyzing an exergonic reaction. Based

on the ATP potential, the quantum yield and the energy

of 633 nm photons, we estimate that ca. 4% of theabsorbed light energy is conserved in the system. The lim-

its of the system have not as yet been reached, nor has the

system been optimized.


12/18


7. CONCLUSION

Supramolecular structures that mimic the antenna,

reaction centre and proton pumps of natural photosyn-

thetic membranes can be designed and synthesized. Arti-

ficial reaction centres demonstrate that rapid charge

separation and relatively slow charge recombination

results in relatively long-lived charge-separated states that

facilitate the use of the energy stored in these states in

homogeneous solution, or even in interfacial reactions.

The ability to carry out photoinduced electron transfer in

media of low dielectric constant, in rigid media and/or at

low temperatures indicates that fullerene-based systems

would be good candidates for applications such as mol-

ecular scale (opto)electronics, sensors or bioenergetics

where photochemistry would have to occur in self-

assembled or LangmuirBlodgett monolayers, in plastics

or gels, in biological or artificial membranes, in micelles,

etc. Large arrays of porphyrin-based antennas can be con-

structed in order to harvest light efficiently. If these arrays

are coupled to reaction centres based on fullerenes such

N

NN

N

H

H

C

O

N

H

Structure 1. (Carotenopurpurin.)

N

NN

N

H

H

C

O

OCH 3

Structure 2. (Purpurin.)


as in hexad 14, supermolecules can be assembled that can

be effective transducers of light energy to potential energy

in the form of charge-separated states. Furthermore, it is

possible to mimic the basic features of energy conversion

in bacterial photosynthetic membranes in a mostly arti-

ficial, bionic construct that employs artificial reaction

centres. Optimization of such systems could provide solar

biological power packs that might be used to drive theenzymatic synthesis of other high-energy or high-value

compounds, or power natural or artificial nanoscale

machines. Both scientific and practical uses of such mod-

ules can be envisioned.

This work was supported by grants from the Department of

Energy (DE-FG03-93ER14404) and the National Science

Foundation (CHE-0078835). This is publication 538 from the

ASU Centre for the Study of Early Events in Photosynthesis.

APPENDIX A

Structures 115.


13/18


N

H

C

O

H3C

Structure 3. (Carotenoid of structure 1.)

N

N

N

N

N

N

NN Zn

O

O O

O

N

O

O

H

C

O

Structure 4. (Carotenophthalocyanine.)

N

N

N

N

N

N

NN Zn

O

O O

O

N

O

O

H

C

O

Structure 5. (Phthalocyanine.)

C

O

N

H

Structure 6. (Carotenoid of structure 2.)


C

O

N

H

H

Structure 7.

NH

NH

N

N

Structure 8.


14/18


NH3C

NH

NH

N

N

Structure 9.

CN

N N

N N

HH

O

N

H

Structure 10.

NNH

HH

C

O

N N

N N

Structure 11.

NN

N N

N N

HH

H

C

O

Structure 12.



15/18


NH

HN

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

Zn

Zn

Zn

Zn

Structure 13.

N

N

N

N

HN

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

N

Zn

Zn

Zn

Zn H

Structure 14.



16/18


N

N

N

NN

O

O

CN

H H

O

C

O

HH C

O

O-

Structure 15.

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Phil Trans R Soc Lond B (2002)

Discussion

J. Barber (Department of Biological Sciences, Imperial Col-

lege, London, UK). Why have you used C60 as an elec-

tron acceptor?

T. A. Moore. Other than being beautiful molecules,

they can also act as multiple electron acceptors. More

importantly, they have low reorganization energies and it

was for this reason that the use of C60 allowed us to gener-ate recombination spin-polarized triplets similar to those

observed in photosynthetic reaction centres.

R. van Grondelle (Department of Biophysics, Free Univer-

sity, Amsterdam, The Netherlands). In your artificial photo-

synthetic systems, the light-harvesting function of

carotenoids is emphasized. In nature, the photoprotective

role of carotenoids seems to be the optimized function.

Please comment.

T. A. Moore. We have, indeed, in the past studied the

protective effect of carotenoids, but in using them as a

functional antenna, we automatically get the protective

effect, bearing in mind that energy tr

phil. trans. r. soc. lond. 2002, 357, 1481

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